The genetic basis of modularity in the development and evolution of the vertebrate dentition

The construction of organisms from units that develop tinder semi-autonomou s genetic control (modules) has been proposed to be an important component of their ability to undergo adaptive phenotypic evolution. The organization of the vertebrate dentition as a system of repeated parts provides an oppo rtunity to study the extent to which phenotypic modules, identified by thei r evolutionary independence from other such units, are related to modularit y in the genetic control of development. The evolutionary history of verteb rates provides numerous examples of both correlated and independent evoluti on of groups of teeth. The dentition itself appears to be a module of the d ermal exoskeleton, from which it has long been under independent genetic co ntrol. Region-specific tooth loss has been a common trend in vertebrate evo lution. Novel deployment of teeth and reacquisition of lost teeth have also occurred, although less frequently. Tooth shape differences within the den tition may be discontinuos (referred to as heterodonty) or graded. The occu rrence of homeotic changes in tooth shape provides evidence for the decoupl ing of tooth shape and location in the course of evolution. Potential mecha nisms for region-specific evolutionary tooth loss are suggested by a number of mouse gene knockouts and human genetic dental anomalies, as well as a c omparison between fully-developed and rudimentary teeth in the dentition of rodents. These mechanisms include loss of a tooth-type-specific initiation signal, alterations of the relative strength of inductive and inhibitory s ignals acting at the time of tooth initiation and the overall reduction in levels of proteins required for the development of all teeth. Ectopic expre ssion of tooth initiation signals provides a potential mechanism for the no vel deployment or reacquisition of teeth; a single instance is known of a g ene whose ectopic expression in transgenic mice can lead to ectopic teeth. Differences in shape between incisor and molar teeth in the mouse have been proposed to be controlled by the region-specific expression of signalling molecules in the oral epithelium. These molecules induce the expression of transcription factors in the underlying jaw mesenchyme that may act as sele ctors of tooth type. It is speculated that shifts in the expression domains of the epithelial signalling molecules might be responsible for homeotic c hanges in tooth shape. The observation that these molecules are regionally restricted in the chicken, whose ancestors were not heterodont, suggests th at mammalian heterodonty may have evolved through the use of patterning mec hanisms already acting on skeletal elements of the jaws. In general, geneti c and morphological approaches identify similar types of modules in the den tition, but the data are not yet sufficient to identify exact correspondenc es. It is speculated that modularity may be achieved by gene expression dif ferences between teeth or by differences in the time of their development, causing mutations to have cumulative effects on later-developing teeth. The mammalian dentition, for which virtually all of the available developmenta l genetic data have been collected, represents a small subset of the dental diversity present in vertebrates as a whole. In particular, teleost fishes may have a much more extensive dentition. Extension of research on the gen etic control or tooth development to this and other vertebrate groups has g reat potential to further the understanding of modularity in the dentition.